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Toxoplasmosis is widespread in human beings and many other warm-blooded animals.(1) Toxoplasma gondii is an obligate intracellular parasite. The 3 means by which it is mainly spread are transplacental transmission, ingestion of infective tissues, and ingestion of food or water contaminated with infective feces (Fig 1).

Figure 1 Diagram of the life cycle of Toxoplasma gondii.

Cats, including wild Felidae, are the only definitive hosts. Cats excrete T gondii oocysts in their feces. Excreted oocysts are nonsporulated and, therefore, are noninfective. After defecation, sporulation (development of infective sporozoites inside the oocyst) requires 1 to 5 days and is dependent on environmental conditions. Oocysts can survive for several months to a year during unfavorable environmental conditions and are remarkably resistant to most disinfectants.(1) Human beings and other animals become infected primarily by ingesting food or water contaminated with oocysts or by ingesting infective animal tissues that contain cysts of T gondii. Currently, methods that could determine whether hosts became infected by ingesting undercooked, cyst-infested tissues or by ingesting food contaminated with oocysts do not exist.

After ingestion of fecal-contaminated food or water by a warm-blooded animal, the oocyst ruptures in the intestine and releases 8 sporozoites. Sporozoites multiply in the intestinal cells and in associated lymph nodes, and tachyzoites (rapidly multiplying forms) are formed. Tachyzoites are dispersed to the rest of the body via blood and lymph, eventually encysting in the brain, skeletal and cardiac muscles, and liver. Encysted T gondii organisms are called bradyzoites or cystozoites (slowly multiplying forms). Cysts are microscopic and survive in tissues for the duration of the life of the host. Tachyzoites are found during the acute phase, whereas encysted bradyzoites (tissue cysts) are often found predominantly in the latent, chronic phase.

After infected tissues are ingested, proteolytic enzymes dissolve the wall of the tissue cyst, releasing the bradyzoites, which infect intestinal epithelial cells of the host. After entry into host cells, bradyzoites transform into tachyzoites. These intracellular tachyzoites may undergo repeated intracellular divisions, but ultimately they are dispersed throughout the body and encyst in tissues. The life cycle of T gondii is completed when tissue cysts are ingested by cats. In the intestine of cats, bradyzoites initiate an enteroepithelial coccidian cycle consisting of an asexual (schizonts) and a sexual (gamonts) cycle. After the male gamont fertilizes the female gamont, a wall develops around the fertilized female gamont to form the oocyst.(2)

Transplacental infection can develop when previously noninfected hosts become infected during pregnancy. Toxoplasma gondii multiplies in the placenta and then spreads to fetal tissues. Although transplacental infection can develop during any stage of gestation, the fetus is affected most severely when the pregnant female becomes infected during the first half of gestation.

Although T gondii can be transmitted when transfusing platelets and erythrocytes and transplanting organs, these modes of transmission are less common than transmission via ingestion of tissues containing bradyzoites or food contaminated with oocysts. However, disseminated forms of toxoplasmosis that are often fatal may result from infections transmitted during organ transplant procedures, because the organ recipients are given treatments that are immunosuppressive.

Cats and Toxoplasmosis

Cats are pivotal in the transmission of T gondii. Because of the risk of transplacental transmission, a major public health concern is that of having cats in the same households as pregnant women. To assess this risk, one needs to understand the means by which cats in the wild become infected with T gondii.

Results of epidemiologic studies indicate that most cats in the wild become infected soon after they are weaned by eating infective animal tissues. During controlled studies, most noninfected cats that are fed tissues containing bradyzoites will shed oocysts, whereas less than half of the cats that are fed oocysts will shed oocysts.(3) Moreover, the number of oocysts shed by a cat after ingestion of oocysts is far fewer than after ingestion of bradyzoites in infective tissues. The ingestion of infected rodents and birds by cats can lead to excretion of large numbers of environmentally resistant oocysts. Transplacental infection can develop in cats, and kittens infected in utero can shed T gondii oocysts after birth.(4,5)

Although cats can shed T gondii oocysts after reinfection (or even without reinfection), the frequency of repetitive shedding of oocysts in cats in the wild is unknown.(6) Under controlled conditions, cats that have shed oocysts usually do not have a second episode of oocyst shedding after a challenge inoculation with T gondii that takes place within 3 to 6 months of the primary infection. How long this immunity to oocyst shedding lasts has not been determined. In an experiment I performed, 4 of 9 cats challenge-inoculated 6 years after a primary infection had a second episode of oocyst shedding.

After super infection with Isospora felis, cats immune to toxoplasmosis have been induced to shed large numbers of T gondii oocysts during a second episode of shedding.(1) Although concomitant infection with feline immunodeficiency virus can affect the severity of toxoplasmosis in cats,(7) it cannot initiate another episode of shedding of oocysts.(8)

Cats often defecate and bury their feces in the hay and food bins of barns or in the soft ground of gardens and flower pots. Generally, feces of cats are hard and may remain in the area for months. Unless cats are sick, little or no feces will stick to their perineal area. Because of their grooming habits, to our knowledge, fecal matter has not been found on the fur of clinically normal cats. Usually, adult cats are not diarrheal during the period that they are shedding oocysts.(1) Therefore, the possibility of transmission to human beings via touching or caring for cats is minimal or nonexistent. The chance of becoming infected via soil contaminated by feral cats probably is greater than the chance of becoming infected via soil contaminated by cats housed indoors, because feral cats usually hunt birds and small mammals in which a sylvatic cycle of T gondii is maintained. Additionally, the prevalence of T gondii infection is higher in feral cats than in domestic cats.

Results of epidemiologic studies based on serologic surveys have been inconclusive in linking the infection of human beings to the fact that cats were in the house. Results of epidemiologic studies for the detection of T gondii oocysts in soil also have been inconclusive in linking specific infections of human beings to cats. However, analysis of results of epidemiologic studies(9) correlating the shedding of oocysts by cats with the cultural habits and rates of T gondii infection in the general human population indicate that cats are involved in epidemiologic aspects of toxoplasmosis. Therefore, appropriate measures should be taken to minimize exposure to oocysts, especially during pregnancy.

Because cats may not develop antibodies to T gondii during the oocyst-shedding period, serologic examination of cats does not provide useful information regarding the ability of a particular cat to transmit toxoplasmosis. However, a cat that is serologically positive for T gondii probably has had a previous episode of oocyst shedding. Thus, serologically positive cats may pose less risk than serologically negative cats; nonetheless, because cats can shed oocysts a second time, appropriate precautions should be taken to prevent contamination of food and water with oocysts, irrespective of the serologic status of the cat.(1)

The number of cats in the United States is increasing steadily and is expected to be 69 million by the year 2000.(10) The number of feral cats probably is greater than that of domestic cats. Toxoplasma gondii oocysts in feces have been detected in < 1% of cats that have been examined in the United States, possibly because oocysts usually are shed for only 1 to 2 weeks during the life of the cat. Because oocysts are small (10 µm)1 and the period of shedding is limited, the chance of detecting T gondii oocysts during routine fecal examination is slight. Toxoplasmosis in pet cats that results from ingesting feral animals or uncooked meat is unpredictable, but a fecal examination is not helpful in determining whether a particular cat is shedding oocysts.

Food Animals and Toxoplasmosis

An estimated 30 to 40% of adult human beings in the United States have antibodies to T gondii.(1,11) Analysis of results of epidemiologic studies suggest that the ingestion of cysts in undercooked or uncooked meat is an important source of T gondii for people in the United States. In one study,(12) the proportion of human beings with T gondii infection was higher in populations that ate undercooked meat than in populations that thoroughly cooked meat before consumption. In another study,(13) 28 of 45 women who delivered a congenitally infected child recalled that they had handled or consumed uncooked meat during gestation. Americans consume 32 kg of beef, 22.5 kg of pork, 0.45 kg of lamb and mutton, and 27.2 kg of poultry annually.(14) About a third to a half of the meat consumed in the United States is processed meat. It is believed that T gondii is killed by salting, curing, or heating procedures used for making processed meat.(15,16) Therefore, properly processed meat is an unlikely source for T gondii infection of human beings. Ingestion of frozen meat probably is of negligible importance in the transmission of toxoplasmosis to human beings, because most of the T gondii tissue cysts will be killed by freezing at temperatures commonly found in ordinary household freezers.(17,18)

Although T gondii infection of sheep is widely prevalent, the public health importance of toxoplasmosis in adult sheep is unknown; in the United States, most meat from adult sheep is not used for human consumption.(19) In one survey,(19) 65% of the ewes on 33 farms had T gondii antibodies in their serum at a 1:64 dilution, as determined by use of the modified agglutination test, and up to 95% of the ewes on certain farms were seropositive. Little is known about the prevalence of T gondii infection in lambs. Results of a California survey that were published in 1977(20) included the fact that 8% of lambs had antibodies to T gondii; however, the prevalence of T gondii infection might be higher in transplacentally infected lambs. In one outbreak of toxoplasmosis on a farm in South Dakota,(21) 80 ewes gave birth to 144 lambs, but 30 of the lambs were born dead. Toxoplasma gondii was detected in 11 of the 30 stillborn lambs. The remaining 114 lambs grew normally, but 68 (59.6%) were seropositive for T gondii; 66 of the 68 lambs had T gondii antibody titers of > 1:256. Eight lambs slaughtered at 7 months of age all had cysts of T gondii in edible tissues of their carcasses. Thus, eating undercooked lamb meat may pose a public health concern for human beings.

Although T gondii cysts may be found in edible tissues of chickens,(22) poultry products probably are not important in the transmission of toxoplasmosis to human beings because they usually are frozen for storage and are thoroughly cooked to avoid diseases that could be caused by contamination with other organisms. The prevalence of T gondii in commercially raised poultry in the United States is unknown. Although T gondii may be found in horses,(1) horse meat is rarely eaten by people in the United States.

Toxoplasma gondii has not been isolated from beef obtained from cattle slaughtered in the United States.(1) The only T gondii isolated was from the intestines of a cow, but organisms were not isolated from any edible tissues.(23) Analysis of results of studies indicate that, in experimental conditions, cattle have high resistance to T gondii infection.(24) Within a few months after inoculation, T gondii organisms usually are not detectable in beef, using bioassays that are useful for detecting T gondii in mice. Bioassays developed for use in cats may be necessary to detect T gondii in beef.(24) In addition, erratic humoral antibody responses of cattle exposed to T gondii organisms make the Sabin-Feldman dye test, indirect hemagglutination test, and latex agglutination test unsuitable for use in the detection of T gondii infection.(25) The agglutination test, using mercaptoethanol, appears to be the most specific test for detecting T gondii infections in cattle.(25) For these reasons, the prevalence of viable T gondii organisms in beef is unknown. Therefore, the importance of beef in the transmission of T gondii infection to people is undetermined, but it is believed that it is not an important source of infection.

By exclusion, fresh pork may be the main meat that is a source of T gondii in the United States. Analysis of results of serologic surveys indicate that T gondii antibodies are widely prevalent in swine in the United States. Analysis of results for a national serologic survey of pigs revealed that T gondii antibodies were found in 2,583 of 11,229 (23%) market-weight pigs and 257 of 613 (42%) adult pigs that were killed for food in 1983 and 1984.(26) A decade later, using the same testing procedures that were used for the national survey of 1983 and 1984, the seroprevalence had declined to 222 of 1,000 (22%) sows from Iowa(27) and 1,056 of 5,080 (20.8%) sows from Illinois.(28) In our experience, the serologic test used had 94% specificity, as viable T gondii organisms were recovered from the hearts of 170 of the 1,000 sows from Iowa. Toxoplasma gondii organisms can survive in living pigs for > 1 year after experimentally induced T gondii infection, including persisting in muscles that comprise the ham, bacon, spareribs, tenderloin, Boston butt, and picnic.(17,29)

Venison and meat from other wild animals also can be sources of T gondii cysts.(1) Toxoplasma gondii organisms have been found in muscles of naturally infected deer,(30) bear,(31) moose, and pronghorn,(32) and T gondii can encyst in elk.(33) The prevalence of black bears in Pennsylvania with T gondii was the highest among all other hosts in the United States, including domestic animals and human beings.(34) Seroprevalence was determined to be about 80% for all black bears tested during each year of the 3 year survey (1991 to 1993). Viable T gondii organisms were isolated from the cardiac tissues of 10 of 28 bears.(35) Thus, wild animal meat can serve as a source of organisms for hunters and their families, especially when care is not taken while eviscerating and handling the game or when meat from these animals is served undercooked or uncooked. More importantly, viscera and meat scraps left at the site of the kill could serve to infect cats and further spread T gondii in the environment.

Toxoplasmosis has developed in human beings that drink unprocessed goat's milk,(36,37) and T gondii has been found in milk of goats that were experimentally inoculated with T gondii.(1) Therefore, goat's milk should be pasteurized before consumption by human beings, particularly infants, who are more susceptible to toxoplasmosis than adults. Toxoplasma gondii may survive longer in infants than in adults because the concentration of proteolytic enzymes in the intestine of infants is less than that in adults. Although the risk of acquiring toxoplasmosis by drinking cow's milk is minimal, it should be pasteurized or boiled to reduce exposure to other milk-transmitted pathogens.

Clinical Toxoplasmosis

Approximately 30% of the women of childbearing age in the United States have antibodies against T gondii and, therefore, are immune to toxoplasmosis.(1) The remaining 70% of the women are at risk of acquiring T gondii infection during pregnancy. Should a noninfected woman acquire T gondii infection during pregnancy, there is a 20 to 50% probability that her fetus will be infected.(11) Estimates of the number of T gondii-infected children born every year in the United States range from 1 infected child/1,000 births to 1 infected child/10,000 births.(11,38) Although most infected children do not have obvious clinical signs at birth, many are likely to have manifestations of the disease later in life (eg, chorioretinitis and mental retardation).(13,39) The estimated annual national cost of raising transplacentally infected children was $5.3 billion in 1993.(40)

Although most postnatally acquired infections are subclinical, manifestations of toxoplasmosis usually include large lymph nodes, headaches, and muscle aches; however, any organ may be affected. Of 37 people in Atlanta that had clinical toxoplasmosis, 33 were febrile, 31 had large lymph nodes and headaches, 22 had muscle aches, and 20 were anorectic and had sore throats.(41) Identical symptoms were described for 31 US soldiers that contracted toxoplasmosis through exposure to contaminated water in the Panama Canal area.(42) Toxoplasmosis was diagnosed in these 2 groups of people because many were affected simultaneously.

Devastating illness may develop in patients with acquired immunodeficiency syndrome (AIDS) and in patients given immunosuppressive treatment for organ transplant or as part of a chemotherapeutic regimen for the treatment of cancer.(43) Signs of encephalitis are the predominant clinical signs of toxoplasmosis in patients with AIDS. It is estimated that 3 to 10% of all patients with AIDS in the United States die of toxoplasmosis on the basis of the fact that 30% of all adults in the United States are seropositive. In Europe and Africa, approximately a fourth to a half of the patients with AIDS develop clinical signs of toxoplasmosis, because, in part, of a higher proportion of seropositive people in the general population.(43)

Toxoplasmosis in people with AIDS results from the reactivation of latent infections. There is no additional danger of transmission of T gondii from their pets. Furthermore, pets are considered to be good companions for people with AIDS.

Clinical signs of toxoplasmosis similar to those observed for human beings also are evident for domestic animals, especially dogs,(1) cats,(44) New World monkeys, and marsupials.(1) New World monkeys and marsupials are highly susceptible to infection with T gondii and rarely survive toxoplasmosis. The most common clinical sign of toxoplasmosis in sheep and goats is abortion, which causes economic losses.(1,45) Sheep that abort as a result of toxoplasmosis do not have subsequent abortions attributable to toxoplasmosis, and, thus, can be used for future breeding.

Prevention and Control

To prevent infection of human beings by T gondii, people should wash their hands thoroughly with soap and water after handling meat. All cutting boards, sink tops, knives, and other utensils that were in contact with uncooked meat should be washed with soap and water, because water will kill the stages of T gondii that are found in meat.(46) Meat should be cooked until a temperature of 66 C (151 F) has been reached before consumption by human beings or other animals, and tasting while cooking meat or seasoning homemade sausages should be avoided.

Pregnant women should avoid contact with cat feces, soil, and uncooked meat. Cat litter should be disposed of every day, preferably by persons other than pregnant women. Gloves should be worn while gardening. Vegetables should be washed thoroughly before eating because of possible contamination with soil that contains cat feces. Expectant mothers should be aware of the dangers of toxoplasmosis. Euthanasia of pet cats will not solve the problem.

Because most cats become infected by eating cyst-contaminated tissues, pet cats should be fed only dry, canned, or cooked food. Cats should never be fed uncooked meat, viscera, or bones, and efforts should be made to keep pet cats indoors to prevent hunting. Because cats cannot use plant sources of vitamin A, some owners feed their cats uncooked liver to improve their fur. This practice should be discontinued, because T gondii cysts frequently are found in livers of food animals,(1) and commercially available cat foods contain most essential nutrients.

Trash containers should be covered to prevent scavenging. Dead animals should be removed promptly to prevent scavenging by pigs(47) and cats. Fetal membranes and dead fetuses of sheep or goats that abort should be handled with caution by persons wearing gloves, and should be buried or incinerated to prevent infection of cats and other animals. Cats should not be allowed near pregnant sheep and goats. Grain should be stored in secure containers to prevent contamination with oocysts.

Dissemination of T gondii oocysts in zoos should be prevented because of the high risk of exposure for children. To prevent infection of zoo animals with T gondii, cats should be housed in a building separate from other animals, particularly marsupials and New World monkeys. As a rule, cats should not be fed uncooked meat; however, if constraints necessitate feeding uncooked meat, frozen meat is less infective than fresh meat, and beef is less likely to contain T gondii tissue cysts than is horse meat, pork, or mutton. Gamma-irradiation can kill tissue cysts without affecting the taste or quality of meat.(48) Brooms, shovels, and other equipment used to clean cat cages and enclosures should be autoclaved or heated to 70 C for at least 10 minutes. While cleaning cages, animal caretakers should wear masks and protective clothing. Feces of cats should be removed daily before oocysts sporulate and become infective.

Vaccines

Objectives for the use of vaccines against toxoplasmosis include reducing fetal damage, reducing the number of T gondii cysts in edible tissues of animals consumed for food, and preventing shedding of oocysts by cats.(49) Achieving all these objectives with the use of a single vaccine currently is not feasible. Although the use of subunit vaccines may be feasible in the future, none is close to becoming approved for commercial use.

One vaccine that contains a strain (S48) of tachyzoites that does not persist in tissues of sheep is available in Europe and New Zealand for use in reducing fetal losses attributable to toxoplasmosis.(45,50) The S48 strain of T gondii is not detectable in tissues of ewes by 4 weeks after inoculation. Vaccination reduces fetal damage attributable to infections that result from challenge-exposure of ewes to field isolates of T gondii; however, it will not prevent infection of the fetus. Ewes vaccinated with the S48-strain vaccine can retain immunity for at least 18 months.(45)

Another strain of T gondii (RH) does not persist in tissues of pigs and induces immunity against T gondii infection.(51) A mutant (ts-4) of the RH strain is also a candidate for use in the development of a vaccine for intermediate hosts, because it grows better at 33 C than it does at 37 C (body temperature).(52) These nonpersistent strains (S48, RH, and ts-4) do not induce oocyst shedding in cats; however, they are live pathogenic organisms that can kill highly susceptible hosts, such as Australian marsupials.(53)

Vaccination of cats to prevent oocyst shedding is altogether different than vaccination of intermediate hosts, because of the 5 asexual stages (types or schizonts) of T gondii that precede the formation of oocysts in the intestine of cats.(1,54) A vaccine that contains live bradyzoites from a mutant strain (T-263) of T gondii has been developed for cats.(55) After oral inoculation with the T-263 strain of bradyzoites, the sexual part of the coccidian cycle is arrested, and only 1 gamont (male or female) develops; thus, oocysts are not produced. The extraintestinal cycle of development in cats inoculated with T-263 brandyzoites is not affected by the mutation. Vaccinating cats with tachyzoites or sporozoites obtained from oocysts other than per oral administration does not induce protective immunity, irrespective of the strain of T gondii used.(53,56) Therefore, developing a noninfective vaccine for the prevention of toxoplasmosis in cats will require maintaining the structure and nature of antigens from the coccidian cycle of T gondii as well as necessitating the oral administration of these antigens. Currently, all attempts at culturing the coccidian phase of T gondii in vitro have been unsuccessful.

References

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2. Dubey JP, Frenkel JK. Cyst-induced toxoplasmosis in cats. J Protozool 1972;19:155-177.

3. Dubey JP, Frenkel JK. Feline toxoplasmosis from acutely infected mice and the development of Toxoplasma cysts. J Protozool 1976;23:537-546.

4. Dubey JP, Carpenter JL. Neonatal toxoplasmosis in littermate cats. J Am Vet Med Assoc 1993;203:1546-1549.

5. Sato K, Iwamoto I, Yoshiki K. Experimental toxoplasmosis in pregnant cats. Jpn J Vet Med Sci 1993;55:1005-1009.

6. Dubey JP, Frenkel JK. Immunity to toxoplasmosis: modification by administration of corticosteriods. Vet Pathol 1974;11:350-379.

7. Davidson MG, Rottman JB, English RV, et al. Feline immunodeficiency virus predisposes cats to acute generalized toxoplasmosis. Am J Pathol 1993;143:1486-1497.

8. Lappin MR, Gasper PW, Rose BJ, et al. Effect of primary phase feline immunodeficiency virus infection on cats with chronic toxoplasmosis. Vet Immunol Immunopathol 1992;35:121-131.

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13. McAuley J, Boyer KM, Patel D, et al. Early and longitudinal evaluations of treated infants and children and untreated historical patients with congenital toxoplasmosis: the Chicago collaborative treatment trial. Clin Infect Dis 1994;18:38-72.

14. Agriculture statistics. In: USDA: Consumption and family living. Washington, DC: US Government Printing Office, 1993;457.

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17. Dubey JP. Long-term persistence of Toxoplasma gondii in tissues of pigs inoculated with T gondii oocysts and effect of freezing on viability of tissue cysts in pork. Am J Vet Res 1988;49:910-913.

18. Kotula AW, Dubey JP, Sharar AK, et al. Effect of freezing on infectivity of Toxoplasma gondii tissue cysts in pork. J Food Prot 1991;54:687-690.

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21. Dubey JP, Kirkbride CA. Economic and public health considerations of congenitial toxoplasmosis in lambs. J Am Vet Med Assoc 1989;195:1715-1716.

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27. Dubey JP, Thulliez P, Powell EC. Toxoplasma gondii in Iowa sows: comparison of antibody titers to isolation of T. gondii by bioassays in mice and cats. J Parasitol 1995; in press.

28. Weigel RM, Dubey JP, Siegel SM, et al. The prevalence of antibodies to Toxoplasma gondii in Illinois swine (1992). J Am Vet Med Assoc, 1994; in press.

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37. Sacks JJ, Roberto RR, Brooks NF. Toxoplasmosis infection associated with raw goat's milk. JAMA 1982;248:1728-1732.

38. Roberts T, Frenkel JK. Estimating income losses and other preventable costs caused by congenital toxoplasmosis in people in the United States. J Am Vet Med Assoc 1990;196:249-256.

39. Guerina NG, Hsu HW, Meissner HD, et al. Neonatal serologic screening and early treatment for congenital Toxoplasma gondii infection. N Engl J Med 1994;330:1858-1863.

40. Roberts T, Murrell KD. Economic losses caused by food-borne parasitic diseases, in Proceedings. Int Symp Cost-benefit Aspects Food Irradiation Processing 1993;51-75.

41. Teutsch SM, Juranek DD, Sulzer A, et al. Epidemic toxoplasmosis associated with infected cats. N Engl J Med 1979;300:695-699.

42. Benenson MW, Takufuji ET, Lemon SM, et al. Oocysttransmitted toxoplasmosis associated with ingestion of contaminated water. N Engl J Med 1982;307:666-669.

43. Luft BJ, Hafner MD, Korzun AH, et al. Toxoplasmic encephalitis in patients with the aquired immunodeficiency syndrome. N Engl J Med 1993;329:995-1000.

44. Dubey JP, Carpenter JL. Histologically confirmed clinical toxoplasmosis in cats: 100 cases (1952-1990). J Am Vet Med Assoc 1993;203:1556-1566.

45. Buxton D. Toxoplasmosis: the first commercial vaccine. Parasitol Today 1993;9:335-337.

46. Jacobs L, Remington JS, Melton ML. The resistance of the encysted form of Toxoplasma gondii. J Parasitol 1982;46:11-21.

47. Dubey JP, Murrell KD, Hanbury RD, et al. Epidemiologic findings on a swine farm with enzootic toxoplasmosis. J Am Vet Med Assoc 1986;189:55-56.

48. Dubey JP, Brake RJ, Murrell KD, et al. Effect of irradiation on the viability of Toxoplasma gondii cysts in tissues of mice and pigs. Am J Vet Res 1986;47:518-522.

49. Araujo FG. Immunization against Toxoplasma gondii. Parasitol Today 1994;10:358-360.

50. Wilkins MF, O'Connell E, Te Punga WA. Toxoplasmosis in sheep III. Further evaluation of the ability of a live Toxoplasma gondii vaccine to prevent lamb losses and reduce congenital infection following experimental oral challenge. N Z Vet J 1988;36:86-89.

51. Dubey JP, Baker DG, Davis SW, et al. Persistence of immunity to toxoplasmosis in pigs vaccinated with a nonpersistent strain of Toxoplasma gondii. Am J Vet Res 1994;55:982-987.

52. Lindsay DS, Blagburn BL, Dubey JP. Safety and results of challenge of weaned pigs given a temperature-sensitive mutant of Toxoplasma gondii. J Parasitol 1993;79:71-76.

53. Lynch MJ, Obendorf DL, Statham P, et al. An evaluation of a live Toxoplasma gondii vaccine in Tammar wallabies (Macropus eugenii). Aust Vet J 1993;70:352-353.

54. Frenkel JK, Smith DD. Immunization of cats against shedding of Toxoplasma oocysts. J Parasitol 1982;68:744-748.

55. Frenkel JK, Pfefferkorn ER, Smith DD, et al. Prospective vaccine prepared from a new mutant of Toxoplasma gondii for use in cats. Am J Vet Res 1991;52:759-763.

56. Freyre A, Choromanski L, Fishback JL, et al. Immunization of cats with tissue cysts, bradyzoites, and tachyzoites of the T-263 strain of Toxoplasma gondii. J Parasitol 1993;79:716-719.

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